Ecological speciation and host adaptation in a parasitic plant

Lead Research Organisation: University of Edinburgh
Department Name: Sch of Biological Sciences

Abstract

A major aim of biological research is to understand how new species evolve. Recent research suggests that adaptation to local environmental differences could be the initial stage in the origin of species in diverse groups such as Heliconius butterflies, radiations of island finches, and Lake Victoria cichlid fish. In this model of ecological speciation, natural selection acts on genetic differences that confer improved fitness for a given climate, soil type, local competitor, herbivore or pathogen, and subsequently these locally adapted populations diverge on a trajectory towards being reproductively isolated species. This model could be important in explaining the origin of new parasite species, as parasites will not only have to adapt to the specific habitat, but the range of hosts within a habitat. However the role of ecological speciation in parasites remains largely untested.

The objective of this research is to test whether ecological speciation underlies the origin of species in a closely related group of generalist parasitic plants. These species can attach to a range of different host plants with a specialised feeding organ and subsequently extract nutrients and water. We will perform experimental and genetic studies on British native eyebrights (Euphrasia), a groups of 21 parasitic species including taxa of high conservation priority. Our previous research has shown species on isolated islands show extensive hybridisation. This research follows on from this finding, by studying Euphrasia on the isolated island of Fair Isle. This island is a mosaic of different habitats, and as such can be used to test the importance of adaptation to contrasting environments, and whether these parasitic species show preferences for different host plants.

We will first test the performance of three ecologically specialised species when grown in different habitats on Fair Isle. To test whether differences in survival reflect adaptation to different hosts, rather than adaptation to other components of the environment, we will grow Euphrasia in an experimental garden site with specific hosts. Finally, we will investigate the genetics of adaptation and speciation by performing genome sequencing of natural populations. This will use high-throughput genomics in conjunction with newer single-molecule sequencing technologies to investigate the genetic changes associated with parasite adaptation.

Overall, our results will give important new insights into the origins of parasitic plant species. Our research tackles this issue from multiple angles, revealing the type of natural selection pressure (such as switching host preferences), as well as the genes underlying this variation. More generally, parasitic plants are keystone species of natural systems, as their parasitic nature reduces the vigour of competitively dominant grasses, and thus maintains grassland species diversity. Our work will show whether ecologically specialised Euphrasia are adapted to different hosts, which may in turn affect their use in grassland management.

Planned Impact

Who will benefit from this research?

Agencies involved in setting priorities for habitat conservation in areas that include taxonomically complex plant groups, such as Euphrasia.

Members of the general public will benefit from a better understanding of native species diversity, how this has evolved, and how this can be conserved.

Horticulturalists and plant growers may benefit from new knowledge on host specificity in hemiparasites.

The residents of Fair Isle will benefit from improved monitoring of their plant diversity.

Early career scientists will benefit from training in new genomic techniques and more generally in biodiversity science.

How will they benefit from this research?

Our research will provide unprecedented insights into the evolution of British native parasitic plants. This in turn will enable us to make clear guidelines for how to conserve this important but often overlooked component of natural ecosystems. We envisage this leading to better informed conservation of rare Euphrasia species, and the preservation of important natural places where these species grow. This may also lead to revised guidelines for ex situ cultivation and reintroductions of hemiparasitic plants.

Our public outreach activities will highlight the importance of parasitic plants in natural ecosystems, and introduce the public to these exciting plants. This will encourage a wider interest in native plant diversity.

Improved knowledge of the importance of environmental preferences, and host ranges, will affect how we cultivate these taxa. In the future, this research could be used to inform best-practice cultivation in natural settings. For example, a Euphrasia species shown to be successful in a particular habitat, or with particular hosts, could be introduced in such an area to reduce the vigour of surrounding plants and maintain ecosystem stability. We have already been approached by seed companies interested in pursuing this route.

Residents of Fair Isle will benefit from continued external investment, making the island a focus for biodiversity monitoring and field studies. This work complements ongoing conservation of birds and marine systems, and may help attract future funding for other conservation actions.

This project will directly support two early career scientists and train them in new and emerging research topics. We also endeavour to supervise project students and pass on this knowledge.

Publications

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Brown M (2021) Student Project: Horticultural protocols for experimental studies of eyebrights (Euphrasia, Orobanchaceae) in Sibbaldia: the International Journal of Botanic Garden Horticulture

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Durán-Castillo M (2022) A phylogeny of Antirrhinum reveals parallel evolution of alpine morphology. in The New phytologist

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Joffard N (2021) Digest: The role of postzygotic isolation in Mimulus speciation. in Evolution; international journal of organic evolution

 
Description We have generated the first reference genome for this plant group. Using this as a resource, we have performed large-scale genome wide sequencing of many populations. This has revealed the evolutionary history of these species on an isolated island. We have also grown many parasitic eyebrights with many hosts, and shown some degree of host specialisation.
Exploitation Route This will form the baseline for future monographic work to define taxon limits, and further evolutionary analyses to understand the origins of plant parasitism and endemic taxa.
Sectors Environment

 
Title A phylogeny of Antirrhinum reveals parallel evolution of alpine morphology 
Description • Parallel evolution of similar morphologies in closely related lineages provides insight into the repeatability and predictability of evolution. In the genus Antirrhinum (snapdragons), as in other plants, a suite of morphological characters are associated with adaptation to alpine environments. • We test for parallel trait evolution in Antirrhinum by investigating phylogenetic relationships using Restriction-site associated DNA (RAD) sequencing. We then associate phenotypic information to our phylogeny to reconstruct patterns of morphological evolution and relate this to evidence for hybridization between emergent lineages. • Phylogenetic analyses show that the alpine character syndrome is present in multiple groups, suggesting that Antirrhinum has repeatedly colonised alpine habitats. Dispersal to novel environments happened in the presence of intraspecific and interspecific gene flow. • We find support for a model of parallel evolution in Antirrhinum. Hybridisation in natural populations, and a complex genetic architecture underlying the alpine morphology syndrome, support an important role of natural selection in maintaining species divergence in the face of gene flow. 
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? Yes  
URL http://datadryad.org/stash/dataset/doi:10.5061/dryad.xgxd254gr
 
Title Eyebright species maintenance (scripts and data accompanying Becher et al., Plant Communications) 
Description This gzipped TAR ball contains data and scripts related to the study on Fair Isle eyebrights by Hannes Becher, Max R. Brown, Gavin Powell, Chris Metherell, Nick J. Riddiford, and Alex D. Twyford, submitted to Plant Communications. Data: genome assembly of Euphrasia arctica, variant call files of the "tetraploid" and "conserved" sets of scaffolds, per-individual k-mer spectra, mapping depths, etc. Scripts: R scripts for the analysis of plant trait data, heterozygosity, ect.; an ipython notebook for the analysis of variant data, and a Mathematica notebook with the derivation of the formulae used to fit pop gen parameters to k-mer spectra. 
Type Of Material Database/Collection of data 
Year Produced 2020 
Provided To Others? Yes  
URL https://zenodo.org/record/3774489
 
Title Eyebright species maintenance (scripts and data accompanying Becher et al., Plant Communications) 
Description This gzipped TAR ball contains data and scripts related to the study on Fair Isle eyebrights by Hannes Becher, Max R. Brown, Gavin Powell, Chris Metherell, Nick J. Riddiford, and Alex D. Twyford, submitted to Plant Communications. Data: genome assembly of Euphrasia arctica, variant call files of the "tetraploid" and "conserved" sets of scaffolds, per-individual k-mer spectra, mapping depths, etc. Scripts: R scripts for the analysis of plant trait data, heterozygosity, ect.; an ipython notebook for the analysis of variant data, and a Mathematica notebook with the derivation of the formulae used to fit pop gen parameters to k-mer spectra. 
Type Of Material Database/Collection of data 
Year Produced 2020 
Provided To Others? Yes  
URL https://zenodo.org/record/3774488
 
Title Genome size, phenotype and population location data for British native eyebrights (Euphrasia) 
Description This dataset includes information on native eyebright plants (Euphrasia, Orobanchaceae) studied and measured at a range of sites across Britain and Ireland, with a special sampling focus on Fair Isle (Shetland, Scotland). Attributes measured are location information (Euphrasia species, coordinates and population description), individual plant trait data (including measures of floral and vegetative traits) and genome sizes. 
Type Of Material Database/Collection of data 
Year Produced 2022 
Provided To Others? Yes  
URL https://catalogue.ceh.ac.uk/id/0a77d3b5-03ce-4a14-ab2d-acc4aa7bd0ef
 
Title Is there hybridisation between diploid and tetraploid Euphrasia in a secondary contact zone? 
Description • Premise of the study: Hybridisation between species with contrasting ploidy is usually considered rare in nature due to strong ploidy related postzygotic reproductive isolating barriers. However, genomic sequencing has revealed previously overlooked examples of natural cross-ploidy hybridisation, suggesting this phenomenon may be more common than once thought. Here, we investigate potential cross-ploidy hybridisation in British eyebrights (Euphrasia, Orobanchaceae), a group where thirteen putative cross-ploidy hybrid combinations have been reported based on morphology. • Methods: We analysed a contact zone between diploid E. rostkoviana and tetraploid E. arctica in Wales. We sequenced part of the internal transcribed spacer of nuclear ribosomal DNA (ITS1) and used Genotyping by Sequencing (GBS) to look for evidence of cross-ploidy hybridisation and introgression. • Key results: All variant sites in the ITS1 region were fixed between diploids and tetraploids, indicating a strong barrier to hybridisation. Clustering analyses of 356 SNPs generated using GBS clearly separated samples by ploidy and revealed strong genetic structure (FST = 0.44). However, the FST distribution across all SNPs was bimodal, indicating potential differential selection on loci between diploids and tetraploids. Demographic inference with dadI suggested potential gene flow - with this limited to around one or fewer migrants per generation. • Conclusions: Our results suggest recent cross-ploidy hybridisation is rare or absent in a site of secondary contact in Euphrasia. While a strong ploidy barrier prevents hybridisation over ecological time-scales, such hybrids may form in stable populations over evolutionary time-scales and may allow for cross-ploidy introgression to take place. 
Type Of Material Database/Collection of data 
Year Produced 2022 
Provided To Others? Yes  
URL http://datadryad.org/stash/dataset/doi:10.5061/dryad.3j9kd51nr
 
Description Collaborative British native plant research with the Royal Botanic Garden Edinburgh 
Organisation Royal Botanic Garden Edinburgh (RBGE)
Country United Kingdom 
Sector Charity/Non Profit 
PI Contribution We have been collaborating in: (1) experimental studies of British native plants, (2) the use of genomics from living plant collections, (3) teaching using RBGE research collections and (4) developing genomic tools to tell plant species apart.
Collaborator Contribution Has provided essential resources including access to plant collections and care of experimental plants.
Impact https://doi.org/10.1111/nph.17752 https://doi.org/10.1098/rstb.2015.0338
Start Year 2014